Justification
Global and European regional assessment: Critically Endangered (CR)
EU 27 regional assessment: Critically Endangered (CR)
Microcondylaea bonellii is a European endemic species. It has lost 84% of its distribution in terms of area of occupancy (AOO) and habitat quality over the last three generations (c. 30 years) and the threats are known and increasing. Therefore, the species is assessed as Critically Endangered (A2c+3c) both globally and for the EU Member States due to inferred population declines of over 80% from the declines in AOO and habitat quality. Furthermore, as the species is becoming increasingly fragmented, the risk of extinction due to isolation/genetic drift/local impacts is also increasing with the projected loss of all Croatian and Italian populations in the next 30 years.
Geographic Range Information
Microcondylaea bonellii is a European endemic species that originally had an extensive range in south-central Europe, where it was found in the northern and eastern tributaries of the Adriatic Sea, from the Po basin south to Greece (Lopes-Lima et al. 2017).
The species is now considered extinct in Switzerland (Rüetschi et al. 2012) and Greece, and has lost much of its former range, as detailed in the population section. In Switzerland whilst the species has not been reported for some time, there have not been sufficient surveys so it is considered possibly extant there for this assessment. A total of 11 subpopulations remain: six small subpopulations are now known in northern Italy, one in Slovenia on the Vipava River, one in Croatia on the Mirna River, one in Montenegro (not mapped) and two in Albania, the last three all belonging to the Skadar/Drin Basin (Mrkvicka 2018, Sousa et al. 2020, Lyubas et al. 2022, N. Riccardi and M. Lopes-Lima pers. obs.). The species is probably also extinct in northern North Macedonia, although further research is needed to confirm this. Extinct regions are not mapped for this species.
Population Information
The latest evidence presented in this assessment shows an 84% decline in area of occupancy (AOO) and habitat quality over the last three generations (approximately 30 years). The first wave of extinctions appears to have occurred before the 1970s, coinciding with industrial development and the intensification of agro-industrialisation. Subsequently, extant subpopulations probably declined due to fragmentation and habitat degradation. Only a few isolated subpopulations have been confirmed by recent surveys (2013–2022).
In Italy, only eight subpopulations (if two eDNA records are included) persist in scattered localities in the north-west and north-east Italian regions (Po, Brenta and Isonzo river basins), typically in streams and canals intensively used for irrigation. The AOO in Italy has decreased by more than 92% in the last 30 years. Populations in the Po tributaries were reduced by more than 95% in abundance due to the prolonged winter drought (2018–2019), the effects of which were probably exacerbated by the increase in the invasive freshwater mussel species Corbicula fluminea, and Sinanodonta woodiana.
In the Balkans, the subpopulations of the Mirna River in Croatia (Mrkvicka 2018) and the Vipava River in Slovenia (Govedič and Govedič 2019) are still present, but also severely impacted. Habitat conditions seem to guarantee better survival chances for subpopulations in the Balkans (e.g. Govedič and Govedič 2019) than in Italy.
The only recent records for Albania and Montenegro are two subpopulations found in 2019 and 2020 both belonging to the Drin River basin (Sousa et al. 2020, Lyubas et al. 2022). The results of genetic analyses (Lopes-Lima pers. comm. 2022; Lyubas et al. 2022) show that these subpopulations are divergent from the Italian/Croatian ones, which have very low genetic diversity (Nagel and Badino 2001, Froufe et al. 2017). Therefore, the populations of the Drin basin should be considered as a unique conservation unit.
Habitat and Ecology Information
Little is known about this species' habitat and ecological requirements or even its biology. It inhabits riverine ecosystems and possibly flowing parts of lakes (although in lakes only shells have been found, possibly transported from rivers), preferably in flowing waters on fine to coarse grained sand, lying in stable banks and eventually overgrown by aquatic plants (Nagel et al. 2007, Lopes-Lima et al. 2017). To date, ecological studies have been limited to some biological characteristics of a single subpopulation (Torrente Versa, northeastern Italy; Nagel et al. 2007), but other information crucial for the conservation of the species, such as the identity of the host fish, is completely lacking.
Microcondylaea bonellii has the typical unique reproductive features of most Unionidae species including larval parental care (i.e. brooding) and larval parasitism on freshwater fish (and occasionally other vertebrates). The species is a short-term breeder capable of consecutive brooding, which is apparently produced in the absence of males. It is not known whether they can store sperm or are cryptic hermaphrodites. Eggs and larvae (glochidia) are brooded in all four gills (Nagel et al. 2007). The release of larvae probably occurs after a few weeks in the form of cylindrical masses (conglutinates) that mimic the prey of the host fish. Although the identity of the host fish is still unknown, the presence of conglutinates suggests a rather narrow host range (Strayer et al. 2004). The glochidia of M. bonellii are D-shaped and small, suggesting that they attach mainly to gills. (Nagel 1999).
Threats Information
The species has shown widespread declines as a result of several major threats, including water pollution, dam construction, drainage, river channelling and sedimentation. The species is likely to be vulnerable to changes in water chemistry as it requires clean water from flowing rivers or wave-exposed lake shores.
Although there are no studies on the sensitivity of Microcondylaea bonelli to pollution, nitrogen compounds, especially ammonia, and temperature fluctuations are suspected to be major stressors, as for other mussel species (Douda 2010, Beggel et al. 2017). In Italy, recent prolonged droughts and artificialisation of river beds are severely affecting the few remaining populations (Riccardi et al. 2022). Periodic monitoring shows that these populations are declining due to the channelling of river beds and prolonged droughts. Increased damming and channelling of the riverbed has almost extirpated the Torrente Versa population, with very few adults remaining in suboptimal conditions (N. Riccardi pers. obs. 2022).
The introduction of alien species has probably contributed substantially to the decline of M. bonellii through competition (e.g. the freshwater bivalves Corbicula fluminea, Sinanodonta woodiana) and predation, such as the crayfish Procambarus clarki, Orconectes limosus, and Pacifastacus leniusculus, and the Muskrat Ondatra zibethicus (Lopes-Lima et al. 2017). The decline of freshwater mussel species is linked to the condition of the native fish populations (Modesto et al. 2018). However, as the host fish are not known, it is difficult to confirm the lack of native hosts as a threat, but given the observed decline of the native freshwater fish fauna in Italy, it is highly likely to be a major threat.
Use and Trade Information
No trade or use is known for this species.
Conservation Actions Information
Microcondylaea bonellii is listed in Annex V of the Habitats Directive (92/43/EEC), which provides protection against non-existing threats, as the species is not exploited. The species is also listed in Appendix III: Protected Fauna Species of the Bern Convention and is protected in the Italian region of Emilia-Romagna: Legge Regionale 15/2006 "Disposizioni per la tutela della fauna minore in Emilia-Romagna". At present, it is not eligible for European conservation funding (e.g. LIFE) due to insufficient risk assessment. In Italy, two of the three rivers in Piedmont, the Rotaldo and the Stura, are included in Natura 2000 sites, but M. bonellii is not listed as a species of Community importance in the Natura 2000 sites in Piedmont (Sindaco et al. 2003). Further legislation, such as the addition of other Annexes to the EU Habitats Directive, should be implemented at regional and national levels to protect and improve the conservation status of the species.
A project to conserve and study the Italian populations of M. bonellii, funded by the Mohamed bin Zayed Species Conservation Fund, ran from 2020-2021. As part of this project, surveys were carried out in 2019–2020 and gravid females were collected for the implementation of a breeding programme, without success, mainly due to the restrictions imposed by COVID-19. There are no other known conservation efforts for this species.
Effective eradication and control of invasive species such as the Chinese Pond Mussel Sinanodonta woodiana, the Asian Clam Corbicula fluminea, the Muskrat Ondatra zibethicus and the crayfish Procambarus clarkii, Orconectes limosus and Pacifastacus leniusculus should be vigorously implemented. A detailed threat analysis should be carried out for each subpopulation and a review of how to control the invasive species and their impact on this native species should be undertaken, which will help to achieve CBD Target 6 for Italy and other range states. This species would also benefit from habitat restoration, such as the restoration of riparian buffers and the rehabilitation of rivers and streams, together with appropriate river management measures, as these should help to reverse the population decline. These potential habitat restoration measures have been listed as Target 2 of the CBD to be achieved by 2030, so this action would meet the CBD requirements for Italy and other range countries, as well as contributing to the recovery of this species.
Research is needed on the ecological requirements, population trends and distribution of M. bonellii. The fish hosts and the main factors limiting the distribution of the species need to be identified, and abundance and population trends need to be regularly surveyed and monitored. Captive breeding and propagation programmes are needed to increase populations, but methodological approaches for captive breeding need to be developed. Further research is required as this would provide a method of supplementing the remaining populations and increasing their numbers, thus this action would meet the CBD requirements for Objective 4 for Italy and other range countries, as well as benefiting the recovery of this species. It is also important to carry out outreach activities to inform the public and all relevant stakeholders of the importance and critical status of the species.
An action plan for the conservation of this species is urgently needed, as is the implementation of conservation measures at all sites where the species still occurs.